Hostname: page-component-78c5997874-fbnjt Total loading time: 0 Render date: 2024-11-04T21:43:19.709Z Has data issue: false hasContentIssue false
  • English
  • Français

Inhibitory effects of an extract from non-host plants on physiological characteristics of two major cabbage pests

Published online by Cambridge University Press:  17 October 2017

M. Dastranj ,
E. Borzoui ,
A. R. Bandani  and
O. L. Franco
M. Dastranj
Affiliation:
Department of Plant Protection, College of Agriculture and Natural Resources, University of Tehran, Karaj, Iran
E. Borzoui
Affiliation:
Department of Plant Protection, Faculty of Agriculture and Natural Resources, University of Mohaghegh Ardabili, Ardabil, Iran
A. R. Bandani*
Affiliation:
Department of Plant Protection, College of Agriculture and Natural Resources, University of Tehran, Karaj, Iran
O. L. Franco
Affiliation:
S-Inova Biotech, Pos-Graduação em Biotecnologia, Universidade Católica Dom Bosco, Campo Grande, MS, Brazil Centro de analises Proteomicas e Bioquimicas, Universidade Católica de Brasilia, Brasilia-DF, Brazil
*
*Author for correspondence Tel.: +98-263-2818705 Fax: +98-263-2238529 E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

The diamondback moth (Plutella xylostella) and small white cabbage butterfly (Pieris rapae) are the two main serious pests of cruciferous crops (Brassicaceae) that have developed resistance to chemical control methods. In order to avoid such resistance and also the adverse effects of chemical pesticides on the environment, alternative methods have usually been suggested, including the use of plant enzyme inhibitors. Here, the inhibitory effects of proteinaceous inhibitors extracted from wheat, canola, sesame, bean and triticale were evaluated against the digestive α-amylases, larval growth, development and nutritional indecs of the diamondback moth and small white cabbage butterfly. Our results indicated that triticale and wheat extracts inhibited α-amylolytic activity in an alkaline pH, which is in accordance with the moth and butterfly gut α-amylase optimum pH. Dose-dependent inhibition of two crucifer pests by triticale and wheat was observed using spectrophotometry and gel electrophoresis. Implementation of specificity studies showed that wheat and triticale-proteinaceous extract were inactive against Chinese and purple cabbage amylase. Triticale and wheat were resistant against insects’ gut proteases. Results of the feeding bioassay indicated that triticale-proteinaceous extract could cause a significant reduction in survival and larval body mass. The results of the nutritional indecs also showed larvae of both species that fed on a Triticale proteinaceous inhibitor-treated diet had the lowest values for the efficiency of conversion of ingested food and relative growth rate. Our observations suggested that triticale shows promise for use in the management of crucifer pests.

Keywords

enzyme–inhibitor interactionsα-amylasePlutella xylostellaPieris rapaeNutritional indecs
Type
Research Papers
Information
Bulletin of Entomological Research , Volume 108 , Issue 3 , June 2018 , pp. 370 - 379
Check for updates
Copyright
Copyright © Cambridge University Press 2017 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Ashouri, S., Pourbad, R.F., Bandani, A. & Dastranj, M. (2015) Inhibitory effects of barley and wheat seed protein on digestive α-amylase and general protease activity of Leptinotarsa decemlineata Say (Coleoptera: Chrysomelidae). Turkish Journal of Entomology 39, 321–332.Google Scholar
Baker, J.E. (1987) Purification of isoamylases from the rice weevil, Sitophilus oryzae (L.) (Coleoptera: Curculionidae), by high-performance liquid chromatography and their interaction with partially-purified amylase inhibitors from wheat. Insect Biochemistry 17, 37–44.Google Scholar
Bandani, A.R. & Butt, T.M. (1999) Insecticidal, antifeedant and growth inhibitory activities of efrapeptins, metabolites of the fungus Tolypocladium. Biocontrol Science and Technology 9, 499–506.Google Scholar
Barbosa, A.E.A.D., Albuquerque, É.V.S., Silva, M.C.M., Souza, D.S.L., Oliveira-Neto, O.B., Valencia, A., Rocha, T.L. & Grossi-de-Sa, M.F. (2010) α-Amylase inhibitor-1 gene from Phaseolus vulgaris expressed in Coffea arabica plants inhibits α-amylases from the coffee berry borer pest. BMC Biotechnology 10, 1.Google Scholar
Bernfeld, P. (1955) α-and β-amylases. Methods in Enzymology 1, 149–154.CrossRefGoogle Scholar
Bignell, D.E. & Anderson, J.M. (1980) Determination of pH and oxygen status in the guts of lower and higher termites. Journal of Insect Physiology 26, 183–188.Google Scholar
Biswas, P.K., Devi, A., Roy, P.K. & Paul, K.B. (1978) Enzyme activity in dormant and nondormant large crabgrass (Digitaria sanguinalis) seeds following hydration. Weed Science 26, 90–93.CrossRefGoogle Scholar
Bolter, C.J. & Jongsma, M.A. (1995) Colorado potato beetles (Leptinotarsa decemlineata) adapt to proteinase inhibitors induced in potato leaves by methyl jasmonate. Journal of Insect Physiology 41, 1071–1078.Google Scholar
Borzoui, E. & Naseri, B. (2016) Wheat cultivars affecting life history and digestive amylolytic activity of Sitotroga cerealella Olivier (Lepidoptera: Gelechiidae). Bulletin of Entomological Research 106, 464–473.Google Scholar
Borzoui, E., Naseri, B. & Namin, F.R. (2015) Different diets affecting biology and digestive physiology of the Khapra beetle, Trogoderma granarium Everts (Coleoptera: Dermestidae). Journal of Stored Products Research 62, 1–7.Google Scholar
Bradford, M.M. (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry 72, 248–254.Google Scholar
Broadway, R.M. (1997) Dietary regulation of serine proteinases that are resistant to serine proteinase inhibitors. Journal of Insect Physiology 43, 855–874.Google Scholar
Carrillo, L., Martinez, M., Alvarez-Alfageme, F., Castañera, P., Smagghe, G., Diaz, I. & Ortego, F. (2011) A barley cysteine-proteinase inhibitor reduces the performance of two aphid species in artificial diets and transgenic Arabidopsis plants. Transgenic Research 20, 305–319.Google Scholar
Chen, M.S., Feng, G., Zen, K.C., Richardson, M., Valdes-Rodriguez, S., Reeck, G.R. & Kramer, K.J. (1992) α-Amylases from three species of stored grain Coleoptera and their inhibition by wheat and corn proteinaceous inhibitors. Insect Biochemistry and Molecular Biology 22, 261–268.Google Scholar
Damalas, C.A. (2011) Review article potential uses of turmeric (Curcuma longa) products as alternative means of pest management in crop production. Plant Omics 4, 136–141.Google Scholar
Dastranj, M., Bandani, A.R. & Mehrabadi, M. (2013) Age-specific digestion of Tenebrio molitor (Coleoptera: Tenebrionidae) and inhibition of proteolytic and amylolytic activity by plant proteinaceous seed extracts. Journal of Asia-Pacific Entomology 16, 309–315.Google Scholar
De Azevedo Pereira, R., Nogueira Batista, J.A., da Silva, M.C.M., Brilhante de Oliveira Neto, O., Zangrando Figueira, E.L., Valencia Jiménez, A. & Grossi-de-Sa, M.F. (2006) An alpha-amylase inhibitor gene from Phaseolus coccineus encodes a protein with potential for control of coffee berry borer (Hypothenemus hampei). Phytochemistry 67, 2009–2016.Google Scholar
Dias, S.C., Da Silva, M.C.M., Teixeira, F.R., Figueira, E.L.Z., de Oliveira-Neto, O.B., de Lima, L.A., Franco, O.L. & Grossi-de-Sa, M.F. (2010) Investigation of insecticidal activity of rye α-amylase inhibitor gene expressed in transgenic tobacco (Nicotiana tabacum) toward cotton boll weevil (Anthonomus grandis). Pesticide Biochemistry and Physiology 98, 39–44.Google Scholar
Dow, J.A. (1992) Ph gradients in lepidopteran midgut. Journal of Experimental Biology 172, 355–375.Google Scholar
Ebrahimi, M., Sahragard, A., Talaei-Hassanloui, R., Kavousi, A. & Chi, H. (2013) The life table and parasitism rate of diadegma insulare (Hymenoptera: Ichneumonidae) reared on larvae of Plutella xylostella (Lepidoptera: Plutellidae), with special reference to the variable Sex ratio of the offspring and comparison of jackknife and bootstrap techniques. Annals of the Entomological Society of America 106, 279–287.Google Scholar
Franco, O., Rigden, D.J., Melo, F.R. & Grossi-de-sa, M.F. (2002) Plant α-amylase inhibitors and their interaction with insect α-amylases structure, function and potential for crop protection. European Journal of Biochemistry 269, 397–412.CrossRefGoogle Scholar
Hemati, S.A., Naseri, B., Ganbalani, G.N., Dastjerdi, H.R. & Golizadeh, A. (2012) Effect of different host plants on nutritional indices of the pod borer, Helicoverpa armigera. Journal of Insect Science 12, 55.Google Scholar
Jongsma, M.A. & Bolter, C. (1997) The adaptation of insects to plant protease inhibitors. Journal of Insect Physiology 43, 885–895.Google Scholar
Kazzazi, M., Bandani, A.R. & Hosseinkhani, S. (2005) Biochemical characterization of α-amylase of the Sunn pest, Eurygaster integriceps. Entomological Science 8, 371–377.CrossRefGoogle Scholar
Kianpour, R., Fathipour, Y., Karimzadeh, J. & Hosseininaveh, V. (2014) Influence of different host plant cultivars on nutritional indices of Plutella xylostella (Lepidoptera: Plutellidae). Journal of Crop Protection 3, 43–49.Google Scholar
Laemmli, U.K. (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227, 680–685.Google Scholar
Mehrabadi, M., Bandani, A.R. & Saadati, F. (2010) Inhibition of Sunn pest, Eurygaster integriceps, α-amylases by α-amylase inhibitors (T-αAI) from Triticale. Journal of Insect Science 10, 1–13.Google Scholar
Mehrabadi, M., Bandani, A.R. & Kwon, O. (2011) Biochemical characterization of digestive α-d-glucosidase and β-d-glucosidase from labial glands and midgut of wheat bug Eurygaster maura (Hemiptera: Scutelleridae). Entomological Research 41, 81–87.Google Scholar
Mehrabadi, M., Bandani, A.R., Mehrabadi, R. & Alizadeh, H. (2012) Inhibitory activity of proteinaceous α-amylase inhibitors from Triticale seeds against Eurygaster integriceps salivary α-amylases: Interaction of the inhibitors and the insect digestive enzymes. Pesticide Biochemistry and Physiology 102, 220–228.Google Scholar
Mehrkhou, F., Mahmoodi, L. & Mouavi, M. (2013) Nutritional indices parameters of large white butterfly Pieris brassicae (Lepidoptera: Pieridae) on different cabbage crops. African Journal of Agricultural Research 8, 3294–3298.Google Scholar
Melo, F.R., Sales, M.P., Pereira, L.S., Bloch, C. Jr, Franco, O.L. & Ary, M.B. (1999) α-Amylase inhibitors from cowpea seeds. Protein Peptide Letter 6, 385–390.Google Scholar
Morton, R.L., Schroeder, H.E., Bateman, K.S., Chrispeels, M.J., Armstrong, E. & Higgins, T.J. (2000) Bean α-amylase inhibitor 1 in transgenic peas (Pisum sativum) provides complete protection from pea weevil (Bruchus pisorum) under field conditions. Proceedings of the National Academy of Sciences 97, 3820–3825.CrossRefGoogle ScholarPubMed
Oliveira-Neto, O.B., Batista, J.A., Rigden, D.J., Franco, O.L., Falcão, R., Fragoso, R.R., Mello, L.V., dos Santos, R.C. & Grossi-de-Sá, M.F. (2003) Molecular cloning of α-amylases from cotton boll weevil, Anthonomus grandis and structural relations to plant inhibitors: an approach to insect resistance. Journal of Protein Chemistry 22, 77–87.Google Scholar
Priya, S., Kaur, N. & Gupta, A.K. (2010) Purification , characterization and inhibition studies of α-amylase of Rhyzopertha dominica. Pesticide Biochemistry and Physiology 98, 231–237.Google Scholar
Saadati, F. & Bandani, A.R. (2011) Effects of serine protease inhibitors on growth and development and digestive serine proteinases of the Sunn pest, Eurygaster integriceps. Journal of Insect Science 11, 1–12.Google Scholar
SAS. (2004). SAS User's Guide Statistics. Cary, NC, SAS Inst., Inc.Google Scholar
Sayyed, A.H., Omar, D. & Wright, D.J. (2004) Genetics of spinosad resistance in a multi-resistant field-selected population of Plutella xylostella. Pest Management Science 60, 827–832.Google Scholar
Schroeder, H.E., Gollasch, S., Moore, A., Tabe, L.M., Craig, S., Hardie, D.C., Chrispeels, M.J., Spencer, D. & Higgins, T. (1995) Bean α-amylase inhibitor confers resistance to the Pea Weevil (Bruchus pisorum) in transgenic peas (Pisum sativum L.). Plant Physiology 107, 1233–1239.CrossRefGoogle Scholar
Shi, M., Zhu, N., Yi, Y. & Chen, X.X. (2013) Four serine protease cDNAs from the midgut of Plutella xylostella and their proteinase activity are influenced by the endoparasitoid, Cotesia vestalis. Archives of Insect Biochemistry and Physiology. 83, 101–114.Google Scholar
Sivakumar, S., Mohan, M., Franco, O.L. & Thayumanavan, B. (2006) Inhibition of insect pest α-amylases by little and finger millet inhibitors. Pesticide Biochemistry and Physiology 85, 155–160.Google Scholar
Svensson, B., Fukuda, K., Nielsen, P.K. & Bønsager, B.C. (2004) Proteinaceous α-amylase inhibitors. Biochimica et Biophysica Acta 1696, 145–156.Google Scholar
Terra, W.R. & Ferreira, C. (2012) Molecular and evolutionary physiology of insect digestion. pp. 93–119 in Parra, J.R.P. (Ed.) Insect Bioecology and Nutrition for Integrated Pest Management. Boca Raton, CRC Press.Google Scholar
Terra, W.R., Ferreira, C. & Baker, J.E. (1996) Compartmentalization of digestion. pp. 206–235 in Lehane, M.J. & Billingsley, P.F. (Eds) Biology of the Insect Midgut. London, Chapman & Hall.Google Scholar
Terra, W.R., Ferreira, C. & De Bianchi, A.G. (1977) Action pattern, kinetical properties and electrophoretical studies of an alpha-amylase present in midgut homogenates from Rhynchosciara americana (Diptera) larvae. Comparative Biochemistry and Physiology Part B: Comparative Biochemistry 56, 201–209.Google Scholar
Valencia, A., Bustillo, A.E., Ossa, G.E. & Chrispeels, M.J. (2000) α-Amylases of the coffee berry borer (Hypothenemus hampei) and their inhibition by two plant amylase inhibitors. Insect Biochemistry and Molecular Biology 30, 207–213.Google Scholar
Waldbauer, G.P. (1968) The consumption and utilization of food by insects. Advances in Insect Physiology 5, 229–288.Google Scholar
Walker, A.J., Ford, L., Majerus, M.E.N., Geoghegan, I.E., Birch, N., Gatehouse, J.A. & Gatehouse, A.M.R. (1998) Characterisation of the mid-gut digestive proteinase activity of the two-spot ladybird (Adalia bipunctata L.) and its sensitivity to proteinase inhibitors. Insect Biochemistry and Molecular Biology 28, 173–180.Google Scholar
Yang, L., Fang, Z., Dicke, M., van Loon, J.J.A. & Jongsma, M. (2009) The diamondback moth, Plutella xylostella, specifically inactivates mustard trypsin inhibitor 2 (MTI2) to overcome host plant defence. Insect Biochemistry and Molecular Biology 39, 55–61.Google Scholar
Zhao, A.J., Li, Y., Collins, H.L., Mau, R.F.L., Thompson, G.D. & Shelton, A.M. (2002) Monitoring and characterization of diamondback moth (Lepidoptera: Plutellidae) resistance to spinosad. Journal of Economic Entomology 95, 430–436.Google Scholar